Tight junctions control lumen morphology via hydrostatic pressure and junctional tension

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Markus Mukenhirn - , Chair of Biophysics, Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Chen Ho Wang - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Tristan Guyomar - , University of Strasbourg, French National Centre for Scientific Research (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Matthew J. Bovyn - , Max Planck Institute of Molecular Cell Biology and Genetics, Max-Planck-Institute for the Physics of Complex Systems, Center for Systems Biology Dresden (CSBD) (Author)
  • Michael F. Staddon - , Max Planck Institute of Molecular Cell Biology and Genetics, Max-Planck-Institute for the Physics of Complex Systems, Center for Systems Biology Dresden (CSBD) (Author)
  • Rozemarijn E. van der Veen - , Leibniz Institute for Molecular Pharmacology (Author)
  • Riccardo Maraspini - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Linjie Lu - , University of Strasbourg, French National Centre for Scientific Research (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Cecilie Martin-Lemaitre - , TUD Dresden University of Technology (Author)
  • Masaki Sano - , Shanghai Jiao Tong University (Author)
  • Martin Lehmann - , Leibniz Institute for Molecular Pharmacology (Author)
  • Tetsuya Hiraiwa - , National University of Singapore, The University of Tokyo (Author)
  • Daniel Riveline - , University of Strasbourg, French National Centre for Scientific Research (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Alf Honigmann - , Clusters of Excellence PoL: Physics of Life, Chair of Biophysics, Max Planck Institute of Molecular Cell Biology and Genetics (Author)

Abstract

Formation of fluid-filled lumina by epithelial tissues is essential for organ development. How cells control the hydraulic and cortical forces to control lumen morphology is not well understood. Here, we quantified the mechanical role of tight junctions in lumen formation using MDCK-II cysts. We found that the paracellular ion barrier formed by claudin receptors is not required for the hydraulic inflation of a lumen. However, the depletion of the zonula occludens scaffold resulted in lumen collapse and folding of apical membranes. Combining quantitative measurements of hydrostatic lumen pressure and junctional tension with modeling enabled us to explain lumen morphologies from the pressure-tension force balance. Tight junctions promote lumen inflation by decreasing cortical tension via the inhibition of myosin. In addition, our results suggest that excess apical area contributes to lumen opening. Overall, we provide a mechanical understanding of how epithelial cells use tight junctions to modulate tissue and lumen shape.

Details

Original languageEnglish
JournalDevelopmental cell
Publication statusAccepted/In press - 2024
Peer-reviewedYes

External IDs

PubMed 39137775

Keywords

Keywords

  • biological physics, lumen morphogenesis, lumen pressure, mechano-biology, myosin contractility, tight junction, tissue hydraulics